Leigh Combrink

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• Andersen, D., Fischer, G., & Combrink, L. (2024). The Alligator and the Mosquito: North American Crocodilians as Amplifiers of West Nile Virus in Changing Climates. Microorganisms, 12(9). doi:10.3390/microorganisms12091898
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  In an age of emerging zoonoses, it is important to understand the intricate system of vectors and reservoirs, or hosts, and their relation to humans. West Nile Virus (WNV) has been detected in a myriad of nonhuman hosts. Transmission of the virus to humans is reliant on amplified seroprevalence within the host, which occurs primarily in birds. However, recent studies have found that other animal groups, including crocodilians, can obtain seroprevalence amplification to levels that make them competent hosts able to transmit WNV to mosquitoes, which can then transmit to humans. Climate change could exacerbate this transmission risk by shifting the distributions of mosquito vectors towards novel geographic ranges. Here, we use maximum entropy models to map the current and future distributions of three mosquito vector species and four crocodilian species in North America to determine the emerging risk of WNV outbreaks associated with changing climates and WNV associated with crocodilians in North America. From our models, we determined that one mosquito species in particular, Culex quinquefasciatus, will increase its distribution across the ranges of all crocodilian species in all tested climate change scenarios. This poses a potential risk to public health for people visiting and living near crocodilian farms and high-density natural crocodilian populations.
• Combrink, L., Humphreys, I. R., Washburn, Q., Arnold, H. K., Stagaman, K., Kasschau, K. D., Jolles, A. E., Beechler, B. R., & Sharpton, T. J. (2023). Best practice for wildlife gut microbiome research: A comprehensive review of methodology for 16S rRNA gene investigations. Frontiers in Microbiology. doi:10.3389/fmicb.2023.1092216
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  Extensive research in well-studied animal models underscores the importance of commensal gastrointestinal (gut) microbes to animal physiology. Gut microbes have been shown to impact dietary digestion, mediate infection, and even modify behavior and cognition. Given the large physiological and pathophysiological contribution microbes provide their host, it is reasonable to assume that the vertebrate gut microbiome may also impact the fitness, health and ecology of wildlife. In accordance with this expectation, an increasing number of investigations have considered the role of the gut microbiome in wildlife ecology, health, and conservation. To help promote the development of this nascent field, we need to dissolve the technical barriers prohibitive to performing wildlife microbiome research. The present review discusses the 16S rRNA gene microbiome research landscape, clarifying best practices in microbiome data generation and analysis, with particular emphasis on unique situations that arise during wildlife investigations. Special consideration is given to topics relevant for microbiome wildlife research from sample collection to molecular techniques for data generation, to data analysis strategies. Our hope is that this article not only calls for greater integration of microbiome analyses into wildlife ecology and health studies but provides researchers with the technical framework needed to successfully conduct such investigations.
• Payne, N., Combrink, L., Kraberger, S., Fontenele, R. S., Schmidlin, K., Cassaigne, I., Culver, M., Varsani, A., & Doorslaer, K. V. (2023). DNA virome composition of two sympatric wild felids, bobcat (Lynx rufus) and puma (Puma concolor) in Sonora, Mexico. Frontiers in Ecology and Evolution. doi:10.3389/fevo.2023.1126149
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  With viruses often having devastating effects on wildlife population fitness and wild mammals serving as pathogen reservoirs for potentially zoonotic diseases, determining the viral diversity present in wild mammals is both a conservation and One Health priority. Additionally, transmission from more abundant hosts could increase the extinction risk of threatened sympatric species. We leveraged an existing circular DNA enriched metagenomic dataset generated from bobcat ( Lynx rufus , n = 9) and puma ( Puma concolor , n = 13) scat samples non-invasively collected from Sonora, Mexico, to characterize fecal DNA viromes of each species and determine the extent that viruses are shared between them. Using the metaWRAP pipeline to co-assemble viral genomes for comparative metagenomic analysis, we observed diverse circular DNA viruses in both species, including circoviruses, genomoviruses, and anelloviruses. We found that differences in DNA virome composition were partly attributed to host species, although there was overlap between viruses in bobcats and pumas. Pumas exhibited greater levels of alpha diversity, possibly due to bioaccumulation of pathogens in apex predators. Shared viral taxa may reflect dietary overlap, shared environmental resources, or transmission through host interactions, although we cannot rule out species-specific host-virus coevolution for the taxa detected through co-assembly. However, our detection of integrated feline foamy virus (FFV) suggests Sonoran pumas may interact with domestic cats. Our results contribute to the growing baseline knowledge of wild felid viral diversity. Future research including samples from additional sources (e.g., prey items, tissues) may help to clarify host associations and determine the pathogenicity of detected viruses.
• Sharpton, T., Combrink, L., Arnold, H., Gaulke, C., & Kent, M. (2021). Erratum to “Harnessing the gut microbiome in the fight against anthelminthic drug resistance” [Curr. Opin. Microbiol. 53 (February) (2020) 26–34] (Current Opinion in Microbiology (2020) 53 (26–34), (S1369527420300217), (10.1016/j.mib.2020.01.017)). Current Opinion in Microbiology, 62. doi:10.1016/j.mib.2021.01.003
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  The publisher regrets that during production a mistake was introduced to one of the figures. The publisher would like to apologise for any inconvenience caused.
• Arnold, H. K., Combrink, L., Gaulke, C. A., Kent, M. S., & Sharpton, T. J. (2020). Harnessing the gut microbiome in the fight against anthelminthic drug resistance. Current Opinion in Microbiology. doi:10.1016/j.mib.2020.01.017
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  Intestinal helminth parasites present major challenges to the welfare of humans and threaten the global food supply. While the discovery of anthelminthic drugs empowered our ability to offset these harms to society, the alarming rise of anthelminthic drug resistance mitigates contemporary efforts to treat and control intestinal helminthic infections. Fortunately, emerging research points to potential opportunities to combat anthelminthic drug resistance by harnessing the gut microbiome as a resource for discovering novel therapeutics and informing responsible drug administration. In this review, we highlight research that demonstrates this potential and provide rationale to support increased investment in efforts to uncover and translationally utilize knowledge about how the gut microbiome mediates intestinal helminthic infection and its outcomes.
• Combrink, L., Downs, C. T., Botha, A., & Combrink, H. J. (2020). Habitat preferences of Southern Ground-hornbills in the Kruger National Park: implications for future conservation measures. Scientific Reports. doi:10.1038/s41598-020-73236-4
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  Abstract Understanding how a species utilises its habitat, and the processes that give rise to its movements and patterns of space use, is critical for its conservation. Southern Ground-hornbills Bucorvus leadbeateri are listed as Endangered in South Africa, as a result of habitat loss and persecution. The National Species Recovery Plan lists reintroductions as a suitable conservation action, but highlights “understanding the exact habitat requirements of Southern Ground-hornbills” as a knowledge gap. In this study, we used tracking data from six Southern Ground-hornbill groups (a total of 37,060 GPS locations) in the Kruger National Park to investigate their seasonal home range differences and habitat preferences. We used first-passage time analysis to determine the scale at which Southern Ground-hornbills concentrate their foraging efforts and whether specific movement behaviours were linked to habitat types. We found marked differences in seasonal home ranges, with all groups showing a range contraction during the breeding season. Grassland and open woodland habitat types were used throughout the year in accordance with their availability within the territory, with grassland, open woodland and dense thicket being favoured habitats for foraging. Our habitat preference results, based on longitudinal GPS data, allowed us to determine ideal habitat ratios (grassland:open woodland:low shrubland of 1.00:6.10:0.09 ha) to assist with the selection of suitable reintroduction sites for Southern Ground-hornbills. With an increasing number of species being threatened with extinction, reintroductions into suitable habitats may be a useful conservation mitigation measure. However, our findings highlight the importance of a thorough understanding of a species’ movement and space use prior to the selection of areas for reintroduction to ensure the establishment and sustainability of these species at these sites.
• Combrink, L., Glidden, C., Beechler, B., Charleston, B., Koehler, A., Sisson, D., Gasser, R., Jabbar, A., & Jolles, A. (2020). Age of first infection across a range of parasite taxa in a wild mammalian population. Biology Letters, 16(2). doi:10.1098/rsbl.2019.0811
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  Newborn mammals have an immature immune system that cannot sufficiently protect them against infectious diseases. However, variation in the effectiveness of maternal immunity against different parasites may couple with temporal trends in parasite exposure to influence disparities in the timing of infection risk. Determining the relationship between age and infection risk is critical in identifying the portion of a host population that contributes to parasite dynamics, as well as the parasites that regulate host recruitment. However, there are no data directly identifying timing of first infection among parasites in wildlife. Here, we took advantage of a longitudinal dataset, tracking infection status by viruses, bacteria, protists and gastro-intestinal worms in a herd of African buffalo (Syncerus caffer) to ask: how does age of first infection differ among parasite taxa? We found distinct differences in the age of first infection among parasites that aligned with the mode of transmission and parasite taxonomy. Specifically, we found that tick-borne and environmentally transmitted protists were acquired earlier than directly transmitted bacteria and viruses. These results emphasize the importance of understanding infection risk in juveniles, especially in host species where juveniles are purported to sustain parasite persistence and/or where mortality rates of juveniles influence population dynamics.
• Combrink, L., Downs, C. T., Botha, A., & Combrink, H. J. (2017). Habitat structure and diversity influence the nesting success of an endangered large cavity-nesting bird, the Southern Ground-hornbill. Koedoe. doi:10.4102/koedoe.v59i1.1438
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  Habitat features can have a profound effect on the nesting success of birds. Savannas are often managed with predators and large herbivores as priority species, with little thought to the many bird species that management decisions could affect. Using a data set spanning seven breeding seasons, we examined how nesting success of Southern Ground-hornbills (SGHs) Bucorvus leadbeateri in the Kruger National Park varied as a result of various environmental and habitat factors within a radius of 3 km surrounding the nest site. Identifying which factors affect nesting success will allow for targeted management efforts to ensure the long-term survival of SGHs both within and outside of protected areas. Habitat structure and diversity of the vegetation surrounding the nest were the most influential factors on SGH nesting success. SGHs require open grassy areas for foraging and areas with large trees for nesting. Savanna habitat drivers such as elephants and fire should be managed to ensure that sufficient large trees are able to establish in the landscape and to control for bush encroachment. This is especially important in areas earmarked for SGH reintroductions. Nest sites of SGHs should be monitored to mitigate any structural changes in the habitat surrounding the nests. Nests should be modified or artificial nest sites provided, where nests have been damaged or lost, to ensure the continued presence of these birds in African savannas.Conservation implications: Habitat structure and diversity surrounding Southern Groundhornbill nests has a significant impact on their nesting success. This highlights the importance of monitoring vegetation change in savanna habitats where they occur. Management of savanna areas should take factors that influence bush encroachment, such as fire and elephants, into account to ensure the long-term persistence of these birds.
• Combrink, L., Downs, C. T., Botha, A., & Combrink, H. J. (2017). Nest temperature fluctuations in a cavity nester, the southern ground-hornbill. Journal of Thermal Biology. doi:10.1016/j.jtherbio.2017.03.003
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  Southern ground-hornbills Bucorvus leadbeateri inhabit savanna and bushveld regions of South Africa. They nest in the austral summer, which coincides with the wet season and hottest daytime temperatures in the region. They are secondary cavity nesters and typically nest in large cavities in trees, cliffs and earth banks, but readily use artificial nest boxes. Southern ground-hornbills are listed as Endangered in South Africa, with reintroductions into suitable areas highlighted as a viable conservation intervention for the species. Nest microclimate, and the possible implications this may have for the breeding biology of southern ground-hornbills, have never been investigated. We used temperature dataloggers to record nest cavity temperature and ambient temperature for one artificial and 11 natural southern ground-hornbill tree cavity nests combined, spanning two breeding seasons. Mean hourly nest temperature, as well as mean minimum and mean maximum nest temperature, differed significantly between southern ground-hornbill nests in both breeding seasons. Mean nest temperature also differed significantly from mean ambient temperature for both seasons. Natural nest cavities provided a buffer against the ambient temperature fluctuations. The artificial nest provided little insulation against temperature extremes, being warmer and cooler than the maximum and minimum local ambient temperatures, respectively. Nest cavity temperature was not found to have an influence on the breeding success of the southern ground-hornbill groups investigated in this study. These results have potentially important implications for southern ground-hornbill conservation and artificial nest design, as they suggest that the birds can tolerate greater nest cavity temperature extremes than previously thought.
• Combrink, L., Downs, C. T., Ramesh, T., & Kalle, R. (2017). Re-establishing the pecking order: Niche models reliably predict suitable habitats for the reintroduction of red-billed oxpeckers. Ecology and Evolution. doi:10.1002/ece3.2787
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  Distributions of avian mutualists are affected by changes in biotic interactions and environmental conditions driven directly/indirectly by human actions. The range contraction of red-billed oxpeckers (Buphagus erythrorhynchus) in South Africa is partly a result of the widespread use of acaracides (i.e., mainly cattle dips), toxic to both ticks and oxpeckers. We predicted the habitat suitability of red-billed oxpeckers in South Africa using ensemble models to assist the ongoing reintroduction efforts and to identify new reintroduction sites for population recovery. The distribution of red-billed oxpeckers was influenced by moderate to high tree cover, woodland habitats, and starling density (a proxy for cavity-nesting birds) with regard to nest-site characteristics. Consumable resources (host and tick density), bioclimate, surface water body density, and proximity to protected areas were other influential predictors. Our models estimated 42,576.88-98,506.98 km2 of highly suitable habitat (0.5-1) covering the majority of Limpopo, Mpumalanga, North West, a substantial portion of northern KwaZulu-Natal (KZN) and the Gauteng Province. Niche models reliably predicted suitable habitat in 40%-61% of the reintroduction sites where breeding is currently successful. Ensemble, boosted regression trees and generalized additive models predicted few suitable areas in the Eastern Cape and south of KZN that are part of the historic range. A few southern areas in the Northern Cape, outside the historic range, also had suitable sites predicted. Our models are a promising decision support tool for guiding reintroduction programs at macroscales. Apart from active reintroductions, conservation programs should encourage farmers and/or landowners to use oxpecker-compatible agrochemicals and set up adequate nest boxes to facilitate the population recovery of the red-billed oxpecker, particularly in human-modified landscapes. To ensure long-term conservation success, we suggest that the effect of anthropogenic threats on habitat distributions should be investigated prior to embarking on a reintroduction program, as the habitat in the historical range may no longer be viable for current bird populations.
• Combrink, L., & Ndlovu, M. (2015). Feeding preferences of Oxpeckers in Kruger National Park, South Africa. Koedoe. doi:10.4102/koedoe.v57i1.1316
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  Oxpeckers reduce tick loads on ungulate hosts, but they are also known to feed on and exacerbate wounds. An understanding of the feeding behaviours and host preferences of these birds is important since they serve as agents of tick control on both domestic and wild ungulates. We conducted an observational study at two sites within the Kruger National Park in South Africa, exploring the feeding preferences of both Red-billed and Yellow-billed Oxpeckers. Oxpeckers’ host preferences, body-location preferences on different hosts, prevalence of feeding and non-feeding behaviours, and frequency of tolerance versus rejection in different hosts were determined. It was found that Yellow-billed Oxpeckers had a smaller range of hosts – typically larger-sized ungulates – and that Red-billed Oxpeckers diversify to smallersized ungulate hosts when in competition with Yellow-billed Oxpeckers. Body-location preferences were generally consistent across sites and across host species. Tick feeding and other host-feeding behaviours (around the eyes, nose, mouth and ears, and anogenital areas) were fairly common. Only six incidents of wound feeding, from a total of 855 observations, were recorded. Tolerance by an ungulate host species was not related to Oxpeckers’ host preferences, suggesting that other factors such as ungulate body size, tick species and tick stages on the host animal may play a significant role in the feeding preferences of Oxpeckers.Conservation implications: It is important to study Oxpeckers’ behavioural feeding preferences so as to better understand their ecology and present distribution, and to determine where they can be reintroduced in future. Reintroduction not only helps with the proliferation of Oxpeckers, but also benefits ungulate hosts through ectoparasite removal and the subsequent control of tick-borne diseases.
• Evans, S. W., Monadjem, A., Roxburgh, L., McKechnie, A. E., Baker, E. M., Kizungu, R. B., Little, I. T., Matsvimbo, F., Mulwa, R. K., Mwizabi, D., Nalwanga, D., Ndang'ang'a, K., & Combrink, L. (2015). Current conservation status of the Blue Swallow Hirundo atrocaerulea Sundevall 1850 in Africa. Ostrich. doi:10.2989/00306525.2015.1047808
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  The global Blue Swallow Hirundo atrocaerulea was classified as Vulnerable in 2010 on account of its small and rapidly declining population estimated at less than 1 500 pairs. We undertook this study to gain a better understanding of the current status and threats facing this migratory species. Three previously unknown areas that might be part of the species' non-breeding range were identified in Kenya and northern Tanzania. Within its breeding range we identified three previously unknown areas of potentially suitable habitat, one in Tanzania and two in Malawi, which require further exploration. Population viability assessment predicted that the Blue Swallow population will decline by 8% in 10 years. The overall probability of extinction of the species in the wild is 3%. Minimum viable population size analysis suggests that a goal for the long-term conservation of the Blue Swallow should be to mitigate current threats that are driving declines such that the population increases to a minimum of 3 600 indivi...
• Combrink, L., Botha, A., Thompson, C., Ronaldson, G. S., & Murn, C. (2013). Population estimates of three vulture species in Kruger National Park, South Africa. Ostrich. doi:10.2989/00306525.2012.757253
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  Vultures are globally threatened, yet reliable population data on these birds are few, thus measuring their response to change is difficult. Kruger National Park (KNP) in South Africa is an importa...
• Murn, C., Combrink, L., Ronaldson, G., Thompson, C., & Botha, A. (2013). Population estimates of three vulture species in Kruger National Park, South Africa. Ostrich, 84(1). doi:10.2989/00306525.2012.757253
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  Vultures are globally threatened, yet reliable population data on these birds are few, thus measuring their response to change is difficult. Kruger National Park (KNP) in South Africa is an important stronghold for many avian species, particularly vultures. In this study we generate population estimates for three vulture species in KNP using two plotless density estimators (PDE): a distance estimator based on nearest-neighbour distance and T-square sampling. We flew aerial censuses over large (c. 3 500 km2) sample areas in two ecogeographically separate parts of KNP and counted vulture nests visible within predetermined transects. In total 416 White-backed Vulture Gyps africanus, 22 Lappet-faced Vulture Torgos tracheliotos and 24 White-headed Vulture Trigonoceps occipitalis nests were recorded. The nearest-neighbour distance PDE performed poorly, and we used a T-square PDE calibrated with aerial survey counts to extrapolate across KNP and estimate breeding population sizes. There are an estimated 904 (95% CI±162) pairs of African White-backed Vultures, 78 (95% CI±18) pairs of Lappet-faced Vultures and 60 (95% CI±13) pairs of White-headed Vultures in KNP. These results provide a basis for investigating how large vultures respond to ecosystem change and understanding their resilience within a broader environmental change scenario. © 2013 Copyright NISC (Pty) Ltd.

Presentations

• Combrink, L., & Andersen, D. (2024). Predictive Modeling of Mosquito Abundance and West Nile Virus Transmission Dynamics: Insights from a Decade of Surveillance in Arizona. The Wildlife Society Conference. Baltimore, Maryland.
• Combrink, L., Andersen, D., & Fischer, G. A. (2024). Biting Insights: Dynamics and Adaptable Modeling of Mosquitoes and Zoonotic Disease Transmission. Border Health: Information for Action Binational Network for Healthy Communities in the Sonora-Arizona Region. Nogales, Mexico.
• Fischer, G. A., Andersen, D., & Combrink, L. (2024). Modeling Avian Hotspots of Potential West Nile Virus Outbreaks: A case study in Coconino County, Arizona. The Wildlife Society Conference. Baltimore, Maryland.
• Payne, N. R., Vargas, K. L., Mollohan, C., Day, R., & Combrink, L. (2024). Exploring microbiomes as biomarkers of health in a wild carnivore. The Wildlife Society Conference.

Poster Presentations

• Andersen, D., Fischer, G. A., & Combrink, L. (2024). The Alligator and The Mosquito: North American crocodilians as amplifiers of West Nile Virus in changing climates. ALVSCE Research Poster Showcase.